The Evolution of Genital Shape Variation in Female Cetaceans
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ORIGINAL ARTICLE doi:10.1111/evo.13395 The evolution of genital shape variation in female cetaceans Dara N. Orbach,1,2,3 Brandon Hedrick,4 Bernd Wursig,¨ 5 Sarah L. Mesnick,6 and Patricia L. R. Brennan2,4 1Department of Biology, Dalhousie University, Life Science Center, 1355 Oxford Street, Halifax, NS B3H 4R2, Canada 2Department of Biological Sciences, Mount Holyoke College, Amherst, Massachusetts 3E-mail: [email protected] 4Department of Biological Sciences, University of Massachusetts-Amherst, Amherst, Massachusetts 5Department of Marine Biology, Texas A&M University at Galveston, Galveston, Texas 6Southwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, La Jolla, California Received June 28, 2017 Accepted November 5, 2017 Male genital diversification is likely the result of sexual selection. Female genital diversification may also result from sexual selection, although it is less well studied and understood. Female genitalia are complex among whales, dolphins, and porpoises, especially compared to other vertebrates. The evolutionary factors affecting the diversity of vaginal complexity could include ontogeny, allometry, phylogeny, sexual selection, and natural selection. We quantified shape variation in female genitalia using 2D geometric morphometric analysis, and validated the application of this method to study soft tissues. We explored patterns of variation in the shape of the cervix and vagina of 24 cetacean species (n = 61 specimens), and found that genital shape varies primarily in the relative vaginal length and overall aspect ratio of the reproductive tract. Extensive genital shape variation was partly explained by ontogenetic changes and evolutionary allometry among sexually mature cetaceans, whereas phylogenetic signal, relative testis size, and neonate size were not significantly associated with genital shape. Female genital shape is diverse and evolves rapidly even among closely related species, consistent with predictions of sexual selection models and with findings in invertebrate and vertebrate taxa. Future research exploring genital shape variation in 3D will offer new insights into evolutionary mechanisms because internal vaginal structures are variable and can form complex spirals. KEY WORDS: Allometry, cetacean, evolution, geometric morphometrics, natural selection, ontogeny, phylogeny, sexual selection, vagina. Research on genital morphology has largely focused on exploring adaptations can be subtle, careful quantification of morpholog- the often extreme morphological variation found in male intro- ical attributes is critical to identify patterns and the underlying mittent organs, with female genitalia considered less variable than evolutionary drivers of variation (Brennan and Prum 2015). males and subsequently not as well studied (Ah-King et al. 2014; Morphological variation in female genitalia, sometimes as- Brennan 2016). This oversight is surprising as morphological sessed concurrently with male genital variation, may reflect sex- variation in male and female genitalia should covary because of ual selection pressures operating during mating via female mate close mechanical interactions during copulation (Brennan and choice, intrasexual male competition, or sexual conflict (Hosken Prum 2015). Recent studies have quantified previously unreported and Stockley 2004; Simmons 2014; Brennan and Prum 2015). In variation in female genital morphology in several taxa, validating addition, morphological variation in female genitalia may also be the value of exploring female reproductive tract morphology influenced by natural selection that prevents interspecific mating (flies, Puniamoorthy et al. 2010; Yassin and Orgogozo 2013; (lock and key hypothesis; Masly 2012), ensures successful ovipo- waterfowl, Brennan et al. 2007; watersnakes, Showalter et al. sition, or facilitates an easy parturition of neonates or egg-laying 2013; cetaceans, Orbach et al. 2017a). Because female genital (Brennan 2016). Female vaginal shapes and structures can also C 2017 The Author(s). Evolution C 2017 The Society for the Study of Evolution. 1 Evolution DARA N. ORBACH ET AL. exhibit ontogenetic variation, as reproductive organs are often predicted to influence cetacean genital shape as interpopulation not functional at birth in vertebrates and change into their adult variation in testes mass and mating systems are known to occur form during sexual maturation (e.g., rats, Berdnikovs et al. 2007; in spinner dolphins (Stenella longirostris; Perrin and Mesnick snakes, Showalter et al. 2013). 2003). Despite findings that vaginal length scales isometrically to Cetaceans (whales, dolphins, and porpoises; 90 extant body length in cetaceans, we predicted that evolutionary allome- species) are a speciose clade of mammals that evolved from a try would affect genital shape variation because of the positively common terrestrial ancestor. Whales, dolphins, and porpoises ex- allometric relationship between vaginal folds and body length hibit a diverse array of adaptations to aquatic living (reviewed in (Orbach et al. 2017a). We also predicted that shared evolutionary Berta et al. 2015), including social organizations ranging from history would affect genital shape because a moderate phyloge- solitary in some large baleen whales to highly gregarious in some netic signal was reported between vaginal length and body length small toothed whales. Their diverse life histories and adaptations, across the cetacean clade (Orbach et al. 2017a) and morpholog- coupled with the unusual genital complexity of females, make ical traits are expected to be more similar among closely related cetaceans a particularly interesting group to investigate patterns species (e.g., Kamilar and Cooper 2013). Sexual and natural selec- of morphological evolution. Recent work on cetaceans has doc- tion can influence genital shape (e.g., Hosken and Stockley 2004; umented widespread variation in female genital structures called Langerhans et al. 2005; Reinhardt 2010; House et al. 2013). Using vaginal folds, which appears to be unparalleled in other mam- testes size as a proxy for postcopulatory competition, we predicted malian taxa (Orbach et al. 2017a). With the exception of ar- that species with larger relative testes (higher sperm competition) tiodactyls, the closest relatives to cetaceans, other mammalian may have longer and narrower vaginas to make insemination groups do not have vaginal folds (Pabst et al., 1998). These folds more difficult. Cetaceans have larger testes-to-body size ratios are muscular protrusions of the vaginal wall into the lumen, and than similar-sized terrestrial mammals, suggesting they engage their function remains unclear (reviewed in Clarke et al. 1994; in sperm competition (Kenagy and Trombulak 1986; Aguilar and Orbach et al. 2017a). The vaginal folds of cetaceans vary in num- Monzon 1992), although there is extensive interspecific variation. ber, thickness, positioning, shape, and size across species and ap- In addition, we predicted that neonate size may influence vaginal pear to be under strong selection pressures because fold lengths shape, so that relatively larger neonates may be associated with a are positively allometric with body size (Orbach et al. 2017a). shorter and wider vagina to facilitate parturition. Finally, because However, quantifying vaginal fold attributes is difficult, as mor- vaginal shape may be under selection from both of these traits phological characteristics may vary within a species (Orbach et al. simultaneously (Brennan and Prum 2015), we examined the in- 2016, 2017a). In addition to these folds, cetacean genitalia vary teraction between relative testes mass, relative neonate size, and across species in the relative length, width, and proportions of the genital shape. cervix and vaginal regions (Fig. 1), herein referred to broadly as genital shape. However, this variation has yet to be systematically described and examined. Material and Methods Studies of shape variation have revolutionized our under- DATA COLLECTION standing of morphological evolution, particularly concerning Reproductive tracts were obtained opportunistically from fresh complex structures. Several studies have used either Fourier anal- (<24 h postmortem) or moderately decomposed deceased female ysis or geometric morphometric approaches to examine shape cetaceans. Sexually immature and mature specimens were col- variation in insect genitalia (Arnqvist 1998; Garnier et al. 2005; lected from marine mammal response networks and research insti- Pizzo et al. 2006; Simmons and Garcia-Gonzalez 2011), and more tutions in the United States, New Zealand, and South Africa under recently, vertebrate genitalia (Evans et al. 2011; Heinen-Kay and government authorization (see Ethics statement). Most specimens Langerhans 2013; Showalter et al. 2013; Simmons and Firman were collected from toothed whales because of their smaller sizes 2014). However, quantitative studies of female genital shape vari- compared to baleen whales. The marine mammal stranding net- ation have not been previously reported in mammals. works provided information on the total body length (Norris 1961) We use a geometric morphometric approach to analyze 2D and sexual maturity state of specimens (based on regional asymp- genital shape variation in female cetaceans. We examine several totic body lengths or presence of corpora albicantia or corpora hypotheses that may explain genital shape variation including on- lutea on the ovaries;